Abstract
Recent research suggested that plants behave differently under combined versus single abiotic and biotic stress conditions in controlled environments. While this work has provided a glimpse into how plants might behave under complex natural conditions, it also highlights the need for field experiments using established model systems. In nature, diverse microbes colonize the phyllosphere of Arabidopsis thaliana, including the obligate biotroph oomycete genus Albugo, causal agent of the common disease white rust. Biotrophic, as well as hemibiotrophic plant pathogens are characterized by efficient suppression of host defense responses. Lab experiments have even shown that Albugo sp. can suppress non-host resistance, thereby enabling otherwise avirulent pathogen growth. We asked how a pathogen that is vitally dependent on a living host can compete in nature for limited niche space while paradoxically enabling colonization of its host plant for competitors? To address this question, we used a proteomics approach to identify differences and similarities between lab and field samples of Albugo sp.-infected and -uninfected A. thaliana plants. We could identify highly similar apoplastic proteomic profiles in both infected and uninfected plants. In wild plants, however, a broad range of defense-related proteins were detected in the apoplast regardless of infection status, while no or low levels of defense-related proteins were detected in lab samples. These results indicate that Albugo sp. do not strongly affect immune responses and leave distinct branches of the immune signaling network intact. To validate our findings and to get mechanistic insights, we tested a panel of A. thaliana mutant plants with induced or compromised immunity for susceptibility to different biotrophic pathogens. Our findings suggest that the biotroph pathogen Albugo selectively interferes with host defense under different environmental and competitive pressures to maintain its ecological niche dominance. Adaptation to host immune responses while maintaining a partially active host immunity seems advantageous against competitors. We suggest a model for future research that considers not only host–microbe but in addition microbe–microbe and microbe–host environment factors.
Highlights
In the wild, plants are exposed simultaneously to a variety of environmental stresses
We focused our analyses on the plant apoplastic space, as it has been shown in previous work that upon biotic and abiotic stress perception there is a massive increase in secretion of defense- or stress-associated proteins into this compartment (Doehlemann and Hemetsberger, 2013; Delaunois et al, 2014)
Taken together the results indicate that Albugo sp. infections have a stronger influence on the colonization of bacteria where sample clustering is more variable and Albugo-infection status correlates to diversity (Agler et al, 2016)
Summary
Plants are exposed simultaneously to a variety of environmental stresses. Arabidopsis thaliana is the best-studied species of flowering plant (Koornneef and Meinke, 2010), but knowledge about how it behaves in the wild on a molecular level is still limited. This is because abiotic and biotic stimuli constantly fluctuate during wild plant growth, limiting replicability of field experiments. To understand, for example, biotic stress responses, lab experiments with single stresses in isolation should be compared to the same stress under natural conditions
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